Metabolic Depression: A Historical Perspective

  • Philip C. WithersEmail author
  • Christine E. Cooper
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 49)


An extended period of inactivity and reduced metabolic rate of many animals and plants, as well as unicellular organisms, has long been recognized by natural historians, e.g., Aristotle and Pliny. Biologists have studied this phenomenon since the 1550s (Gessner) and 1700s (Van Leeuwenhoek, Buffon). The period of inactivity can be less than a day, a few consecutive days or weeks, an entire season, or even many years. It can involve very different physiological states in response to a variety of environmental stimuli, such as extreme temperatures or unavailability of food or water. These periods of inactivity have been described and classified according to the group of organisms in question, extent and duration of the metabolic depression, ambient and body temperatures, state of body water (frozen or hyperosmotic), or availability of oxygen. Cryptobiosis, or “hidden life,” is an extreme form of inactivity, with often complete cessation of metabolism. It was first described in the 1700s, was further characterized in the 1800s, and in the 1900s physiological studies delineated the extent of metabolic depression. Molecular mechanisms for cryptobiosis have been sought since the late 1900s. Cryptobiosis includes three physiological states, anhydrobiosis (desiccation), osmobiosis (high osmotic concentration), and cryobiosis (freezing), where metabolic depression is associated with an altered physical state of cell water and often involves accumulation of compatible solutes, and one physiological state, anoxybiosis (anoxia), where metabolic depression occurs at the normal cellular hydration state. Dormancy (torpor) is a less extreme form of inactivity, associated with a moderate reduction in metabolic rate (hypometabolism). Although first described by Aristotle and Pliny, studies in the 1900s delineated the basic physiological changes that accompany dormancy. Dormancy allows avoidance of unfavorable short- or long-term climatic conditions and conservation of energy and water. Hibernation is long-term multiday torpor during winter, whereas aestivation is dormancy during summer. In ectotherms, the metabolic depression that accompanies dormancy is intrinsic, with metabolic rate declining to about 10 to 20% of resting metabolic rate at the same body temperature. The molecular mechanisms for intrinsic metabolic depression are poorly understood. In endotherms, torpor involves a fundamental physiological change in body temperature regulation that markedly reduces metabolic rate and water loss, often to <10% of the normothermic resting metabolic rate at the same ambient temperature. Most of this reduction in metabolic rate reflects the decreased setpoint for thermoregulation resulting in reduced metabolic heat production and a Q10 effect; there may be some intrinsic molecular-based metabolic depression in some hibernators. Dormancy allows species to exploit ephemeral environments and colonise habitats that would otherwise be unsuitable for growth or survival at certain times of the year. There are costs to dormancy, but for many species, the energetic and hygric advantages outweigh these costs.


Metabolic Rate Torpor Bout Evaporative Water Loss Metabolic Heat Production Daily Torpor 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Carlos Navas and José Eduardo de Carvalho for their invitation to contribute to this book, Ariovaldo P. Cruz Neto for valuable discussion, and the reviewer for useful comments on the draft manuscript


  1. Aarset AV (1982) Freezing tolerance in intertidal invertebrates (a review). Comp Biochem Physiol A 73:571–580Google Scholar
  2. Abe AS (1995) Aestivation in South American amphibians and reptiles. Braz J Med Biol Res 28:1241–1247PubMedGoogle Scholar
  3. Abe AS, Buck N (1985) Oxygen uptake of active and aestivating earthworm Glossoscolex paulistus (Oligochaeta, Glossoscolecidae). Comp Biochem Physiol A 81:63–66Google Scholar
  4. Anonymous (2003) Glossary of terms for thermal physiology. J Therm Biol 28:75–106Google Scholar
  5. Baker FC (1934) A conchological Rip Van Winkle. Nautilus 48:5–6Google Scholar
  6. Baker H (1753) Employment for the Microscope. Dodsley, LondonGoogle Scholar
  7. Barclay RMR, Lausen CL, Hollis L (2001) What’s hot and what’s not: defining torpor in free-ranging birds and mammals. Can J Zool 79:1885–1890Google Scholar
  8. Becquerel P (1907) Recherché sur la vie latent des grains. Ann Sci Nat (9e s. Bot) 5:193–311Google Scholar
  9. Buffenstein R (1985) The effect of starvation, food restriction and water deprivation on thermoregulation and average daily metabolic rates in Gerbillus pusillus. Physiol Zool 58:320–328Google Scholar
  10. Carpenter RE (1969) Structure and function of the kidney and the water balance of desert bats. Physiol Zool 42:288–302Google Scholar
  11. Christian KA, Corbett LK, Green B (1995) Seasonal activity and energetics of two species of varanid lizards in tropical Australia. Oecologia 103:349–357Google Scholar
  12. Christian KA, Green B, Kennett R (1996) Some physiological consequences of aestivation by freshwater crocodiles, Crocodylus johnstoni. J Herpetol 30:1–9Google Scholar
  13. Churchill TA, Storey KB (1996) Organ metabolism and cryoprotectant synthesis during freezing in spring peepers Pseudacris crucifer. Copeia 1996:517–525Google Scholar
  14. Claussen DL, Townsley MD, Bausch RG (1990) Supercooling and freeze tolerance in the European wall lizard, Podarcis muralis. J Comp Physiol B 160:137–143Google Scholar
  15. Clegg JS (1975) Metabolic consequences and the extent and disposition of the aqueous intracellular environment. J Exp Zool 215:303–313Google Scholar
  16. Clegg JS (1976) Interrelationships between water and metabolism in Artemia cysts–III. Respiration. Comp Biochem Physiol A 53:89–93PubMedGoogle Scholar
  17. Clegg JS (1997) Embryos of Artemia franciscana survive four years of continuous anoxia: the case for complete metabolic rate depression. J Exp Biol 200:467–475PubMedGoogle Scholar
  18. Clegg JS (2001) Cryptobiosis – a peculiar state of biological organization. Comp Biochem Physiol B 128:613–624PubMedGoogle Scholar
  19. Clegg JS, Drinkwater LE, Sorgloos P (1996) The metabolic status of diapauses embryos of Artemia franciscana. Physiol Zool 69:49–66Google Scholar
  20. Coles GC (1968) The termination of aestivation in the large freshwater snail Pila ovate (Ampularidae) – I. Changes in oxygen uptake. Comp Biochem Physiol 25:517–522PubMedGoogle Scholar
  21. Cooper CE, Geiser F (2008) The “minimum boundary curve for endothermy” as a predictor of heterothermy in mammals and birds: a review. J Comp Physiol B 178:1–8PubMedGoogle Scholar
  22. Cooper CE, Geiser F, McAllan B (2005) Effect of torpor on the water economy of an arid-zone dasyurid, the stripe-faced dunnart (Sminthopsis macroura). J Comp Physiol B 175:323–328PubMedGoogle Scholar
  23. Cooper CE, Kortner G, Brigham M, Geiser F (2008) Body temperature and activity patterns of free-living laughing kookaburras: the largest kingfisher is herterothermic. Condor 110:110–115Google Scholar
  24. Cooper CE, Withers PC, Cruz-Neto AP (2009) Metabolic, ventilatory and hygric physiology of the gracile mouse opossum (Gracilinanus agilis). Physiol Biochem Zool 82:153–162PubMedGoogle Scholar
  25. Costanzo JP, Grenot C, Lee RE (1995) Supercooling, ice inoculation and freeze tolerance in the European common lizard, Lacerta vivipara. J Comp Physiol B 165:238–244Google Scholar
  26. Costanzo JP, Claussen DL, Lee RE (1988) Natural freeze tolerance in a reptile. Cryo Letters 9:380–385Google Scholar
  27. Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Hibernation in a tropical primate. Nature 429:825–826PubMedGoogle Scholar
  28. Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2005) Hibernation in the tropics: lessons from a primate. J Comp Physiol B 175:147–155PubMedGoogle Scholar
  29. Davis DE (1976) Hibernation and circannual rhythms of food consumption in marmots and ground squirrels. Q Rev Biol 54:477–514Google Scholar
  30. Davis WH (1970) Hibernation: ecology and physiological ecology. In: Wimsatt WA (ed) Biology of Bats, vol 1. Academic, New York, pp 266–300Google Scholar
  31. Delaney RG, Lahiri S, Fishman AP (1974) Aestivation in the African lungfish Protopterus aethiopicus: cardiovascular and respiratory functions. J Exp Biol 61:111–128PubMedGoogle Scholar
  32. Dinkelacker SA, Costanzo JP, Lee RE (2005) Anoxia tolerance and freeze tolerance in hatchling turtles. J Comp Physiol B 175:209–217PubMedGoogle Scholar
  33. Donohoe PH, Boutilier RG (1998) The protective effects of metabolic rate depression in hypoxic cold submerged frogs. Respir Physiol 111:325–336PubMedGoogle Scholar
  34. Donohoe PH, West TG, Boutilier RG (1998) Respiratory, metabolic, and acid-base correlates of aerobic metabolic rate reduction in overwintering frogs. Am J Physiol 274:R704–R710PubMedGoogle Scholar
  35. Duman JG, Wu DW, Xu L, Tursman D, Olsen TM (1991) Adaptations of insects to subzero temperatures. Q Rev Biol 66:387–410Google Scholar
  36. Eisentraut M (1934) Der winterschlaf der fledermäuse mit besonderer berücksichtigung der wärme-regulation. Z Morph Ökol 29:231–267Google Scholar
  37. Etheridge K (1990) The energetics of aestivating sirenid salamanders (Siren lacertina and Pseudobranchus striatus). Herpetologica 46:407–414Google Scholar
  38. Ewart AJ (1908) On the longevity of seeds. Proc Roy Soc Vict 21:1–210Google Scholar
  39. Florant GL, Heller HC (1977) CNS regulation of body temperature in euthermic and hibernating marmots (Marmota flaviventris). Am J Physiol 232:R203–R208PubMedGoogle Scholar
  40. Gavaret J (1859) Quelques experiences sur les rotifers, les tardigrades et les anguillules des mousses des toits. Ann Sci Nat Zool 11:315–330Google Scholar
  41. Geiser F, Coburn DK, Körtner G, Law BS (1996) Thermoregulation, energy metabolism, and torpor in blossom-bats Synconycteris australis (Megachiroptera). J Zool 239:583–590Google Scholar
  42. Geiser F (1988) Reduction of metabolism during hibernation and daily torpor in mammals and birds: temperature effect or physiological inhibition? J Comp Physiol B 158:25–37PubMedGoogle Scholar
  43. Geiser F (1994) Hibernation and daily torpor in marsupials: a review. Aust J Zool 42:1–16Google Scholar
  44. Geiser F (2004a) Metabolic rate and body temperature reduction during hibernation and daily torpor. Ann Rev Physiol 66:239–274Google Scholar
  45. Geiser F (2004b) The role of torpor in the life of Australian arid zone mammals. Aust Mammal 26:125–134Google Scholar
  46. Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol Zool 68:935–966Google Scholar
  47. Geiser F, Goodship N, Pavey CR (2002) Was basking important in the evolution of mammalian endothermy? Naturwissenschaften 89:412–414PubMedGoogle Scholar
  48. Glasheen JS, Hand SC (1989) Metabolic heat dissipation and internal solute levels of Artemia embryos during changes in cell-associated water. J Exp Biol 145:263–282Google Scholar
  49. Glazer I, Salame L (2000) Osmotic survival of the entomopathogenic nematode Steinernema carpocapsae. Biol Control 18:251–257Google Scholar
  50. Gregory PT (1982) Reptilian hibernation. In: Gans C, Pough FH (eds) Biology of the Reptilia. Academic Press, London, pp 53–154Google Scholar
  51. Guppy MG, Withers PC (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev 7:1–40Google Scholar
  52. Hailey A, Loveridge JP (1997) Metabolic depression during dormancy in the African tortoise Kinixys spekii. Can J Zool 75:1328–1335Google Scholar
  53. Hartner WC, South FE, Jacobs HK, Luecke RH (1971) Preoptic thermal stimulation and temperature regulation in the marmot (M. flaviventris). Cryobiology 8:312–313Google Scholar
  54. Heller HC, Colliver GW (1974) CNS regulation of body temperature during hibernation. Am J Physiol 227:583–589PubMedGoogle Scholar
  55. Heller HC, Walker JM, Florant GL, Glotzbach SF, Berger RJ (1978) Sleep and hibernation: electrophysiological and thermoregulatory homologies. In: Wang LC, Hudson JW (eds) Strategies in the Cold: Natural Torpidity and Thermogenesis. Academic, London, pp 225–265Google Scholar
  56. Hillman SS, Withers PC, Drewes RC, Hillyard S (2008) Ecological and environmental physiology of amphibians. Oxford University Press, OxfordGoogle Scholar
  57. Hochachka PW, Lutz PL (2001) Mechanism, origin, and evolution of anoxia tolerance in animals. Comp Biochem Physiol B 130:435–459PubMedGoogle Scholar
  58. Hudson JW (1978) Shallow daily torpor: a thermoregulatory adaptation. In: Wang LC, Hudson JW (eds) Strategies in the Cold: Natural Torpidity and Thermogenesis. Academic, London, pp 67–108Google Scholar
  59. Jackson DC (1968) Metabolic depression and oxygen depletion in the diving turtle. J Appl Physiol 24:503–509PubMedGoogle Scholar
  60. Jackson DC (2000) Living without oxygen: lessons from the freshwater turtle. Comp Biochem Physiol A 125:299–315Google Scholar
  61. Jaeger EC (1948) Does the poor-will “hibernate”? Condor 50:45–46Google Scholar
  62. Jaeger EC (1949) Further observations on the hibernation of the poor-will. Condor 51:105–109Google Scholar
  63. Kayser C (1961) The Physiology of Natural Hibernation. Pergamon, LondonGoogle Scholar
  64. Keilin D (1959) The problem of anabiosis or latent life: history and current concept. Proc Roy Soc Lond 150:149–191Google Scholar
  65. Keister M, Buck J (1964) Respiration: some exogenous and endogenous effects on rate of respiration. In: Rockstein R (ed) The physiology of the Insecta, vol III. Academic Press, New York, pp 617–658Google Scholar
  66. Kennett R, Christian K (1994) Metabolic depression in estivating long-neck turtles (Chelodina rugosa). Physiol Zool 67:1087–1102Google Scholar
  67. Lasiewski RC (1964) Body temperatures, heart and breathing rate and evaporative water loss in humming birds. Physiol Zool 37:212–223Google Scholar
  68. Laverack MS (1963) The Physiology of Earthworms. Pergamon, OxfordGoogle Scholar
  69. Lee AK, Mercer EH (1967) Cocoon surrounding desert-dwelling frogs. Science 157:87–88PubMedGoogle Scholar
  70. Lees AD (1955) The Physiology of Diapause in Arthropods. Cambridge University Press, CambridgeGoogle Scholar
  71. Lees AD (1956) The physiology and biochemistry of diapauses. Ann Rev Entomol 1:1–16Google Scholar
  72. Loomis SH (1987) Freezing in intertidal invertebrates. Cryo Letters 8:186–195Google Scholar
  73. Lyman CP (1948) The oxygen consumption and temperature regulation of hibernating hamsters. J Exp Zool 109:55–78PubMedGoogle Scholar
  74. Lyman CP (1970) Thermoregulation and metabolism in bats. In: Wimsatt WA (ed) Biology of Bats, vol 1. Academic, New York, pp 301–330Google Scholar
  75. Lyman CP (1978) Natural torpidity, problems and perspectives. In: Wang LC, Hudson JW (eds) Strategies in the Cold: Natural Torpidity and Thermogenesis. Academic, London, pp 9–19Google Scholar
  76. Lyman CP, Willis JS, Malan A, Wang LC (1982) Hibernation and Torpor in Mammals and Birds. Academic, New YorkGoogle Scholar
  77. MacMillen RE (1965) Aestivation in the cactus mouse Peromyscus eremicus. Comp Biochem Physiol 16:227–248PubMedGoogle Scholar
  78. MacMillen RE, Greenaway P (1978) Adjustments of energy and water metabolism to drought in an Australian arid-zone crab. Physiol Zool 51:239–240Google Scholar
  79. Mayhew WW (1965) Hibernation in the horned lizard, Phrynosoma m’calli. Comp Biochem Physiol 16:103–119PubMedGoogle Scholar
  80. McAtee WL (1947) Torpidity in birds. Am Midl Nat 38:191–206Google Scholar
  81. McClanahan LL (1967) Adaptations of the spadefoot toad, Scaphiopus couchi, to desert environments. Comp Biochem Physiol 20:73–99Google Scholar
  82. McClanahan LL, Ruibal R, Shoemaker VH (1983) Rate of cocoon formation and physiological its correlates in a ceratophryid frog. Physiol Zool 56:430–435Google Scholar
  83. McKechnie AE, Lovegrove BG (2002) Avian facultative hypothermic responses: a review. Condor 104:705–724Google Scholar
  84. Mills SC, South FE (1972) Central regulation of temperatue in hibernation and normothermia. Cryobiology 9:393–403PubMedGoogle Scholar
  85. Moberley WR (1963) Hibernation in the desert iguana, Dipsosaurus dorsalis. Physiol Zool 36:152–160Google Scholar
  86. Mrosovsky N (1971) Hibernation and Hypothalamus. Appleton-Century-Crofts, New YorkGoogle Scholar
  87. Mrosovsky N (1990) Rheostasis. The Physiology of Change. Oxford University Press, New YorkGoogle Scholar
  88. Nagy KA, Medica PA (1986) Physiological ecology of desert tortoises in southern Nevada. Herpetologica 42:73–92Google Scholar
  89. Nagy KA, Shoemaker VH (1975) Energy and nitrogen budgets of the free-living desert lizard Sauromalus obesus. Physiol Zool 48:252–262Google Scholar
  90. Needham JT (1743) A letter concerning chalky tubulous concretions, with some microscopical observations on the farina of the red lily, and on worms discovered in smutty corn. Phil Trans R Soc Lond 42:634–641Google Scholar
  91. Nelson DR (2002) Current status of the Tardigrada: evolution and ecology. Integr Comp Biol 42:652–659Google Scholar
  92. Ohga I (1923) On the longevity of the fruits of Nelumbo nucifera. Bot Mag Tokyo 37:87Google Scholar
  93. Pearson OP (1960) Torpidity in birds. In: Lyman CP, Dawe AR (eds) Mammalian Hibernation. Bull Mus Comp Zool 124:93–103Google Scholar
  94. Pedler S, Fuery CJ, Withers PC, Flanigan J, Guppy M (1996) Effectors of metabolic depression in an estivating pulmonate snail (Helix aspersa): whole animal and in vitro tissue studies. J Comp Physiol 166:375–381Google Scholar
  95. Podrabsky JE, Hand SC (1999) The bioenergetics of embryonic diapause in an annual killifish, Austrofundulus limnaeus. J Exp Biol 202:2567–2580PubMedGoogle Scholar
  96. Podrabsky JE, Carpenter JF, Hand SC (2001) Survival of water stress in annual killifish embryos: dehydration avoidance and egg envelope amyloid fibers. Am J Physiol Int Comp Physiol 280:R123–R131Google Scholar
  97. Preyer W (1891) Uber de anabiose. Biol Zbl 11:1–5Google Scholar
  98. Pusey BJ (1990) Seasonality, aestivation and the life history of the salamander fish Lepidogalaxias salamandroides (Pisces: Lepidogalaxiidae). Environ Biol Fishes 29:15–26Google Scholar
  99. Rakshpal R (1962) Respiratory metabolism during embryogenesis of a diapauses species of field cricket, Gryllus pennsylvanicus Burmeister (Orthoptera: Gryllidae). J Insect Physiol 8:217–221Google Scholar
  100. Rasmussen AT (1916) Theories of hibernation. Am Nat 50:609–625Google Scholar
  101. Réaumur RA (1737) Des chenilles qui vivent en société. In: Mortier P (ed) Mémoires pour servir á l’Histoire des Insectes, vol 2. Pierre Mortier, Amsterdam, pp 153–225Google Scholar
  102. Rebecchi L, Altiero T, Guidetti R (2007) Anhydrobiosis: the extreme limit of desiccation tolerance. Invert Surv J 4:65–81Google Scholar
  103. Reeder WG (1949) Hibernating temperature of the bat, Myotis californicus pallidus. J Mamm 30:51–53Google Scholar
  104. Righi G (1972) Bionomic considerations upon the Glossoscoleidae (Oligochaeta). Pedobiologia 12:254–260Google Scholar
  105. Ring RA (1981) The physiology and biochemistry of cold tolerance in Arctic insects. J Therm Biol 6:219–229Google Scholar
  106. Ruschi A (1949) Observations on the Trochilidae. Bull Mus Biol Prof Mello-Leitão, vol 7. Santa Teresa, BrazilGoogle Scholar
  107. Schmid WD (1982) Survival of frogs in low temperature. Science 215:697–698PubMedGoogle Scholar
  108. Schmidt P (1948) Anabiosis. USSR Acadamey of Science, Moscow and LeningradGoogle Scholar
  109. Seidel ME (1978) Terrestrial dormancy in the turtle Kinosternum flavescens: respiratory metabolism and dehydration. Comp Biochem Physiol A 61:1–4Google Scholar
  110. Seymour RS (1973) Energy metabolism of dormant spadefoot toads (Scaphiopus). Copeia 1973:435–445Google Scholar
  111. Smith HW (1930) Metabolism of the lungfish Protopterus aethiopicus. J Biol Chem 88:97–130Google Scholar
  112. South FE, Breazile JE, Dellman HD, Epperly AD (1969) Sleep, hibernation and hypothermia in the yellow-bellied marmot (M. flaviventris). In: Mussacchia XJ, Saunders JF (eds) Depressed Metabolism. New York, Elsevier, pp 277–312Google Scholar
  113. Spallanzani L (1776) Opuscoli di fisica animale e vegetabile. Societa Tipografica (Modena) 2:203–285Google Scholar
  114. Spencer B (1896) Report on the work of the Horn scientific expedition to Central Australia. Part II. Zoology. Dulau, LondonGoogle Scholar
  115. Steiner G, Albin FE (1946) Rescusitation of the nematode Tylenchis polyhypnus sp., after almost 39 years’ dormancy. J Wash Acad Sci 36:97–99PubMedGoogle Scholar
  116. Storey KB (1996) Metabolic adaptations supporting anoxia tolerance in reptiles: recent advances. Comp Biochem Physiol B 113:23–35PubMedGoogle Scholar
  117. Storey KB (2001) Molecular Mechanisms of Metabolic Arrest. Life in Limbo. Bios Scientific, OxfordGoogle Scholar
  118. Storey KB, Storey JM (1986) Freeze tolerant frogs: cryoprotectants and tissue metabolism during freeze/thaw cycles. Can J Zool 64:49–56Google Scholar
  119. Storey KB, Storey JM (1988) Freeze tolerance in animals. Physiol Rev 68:27–84PubMedGoogle Scholar
  120. Storey KB, Storey JM (1989) Freeze tolerance and freeze-avoidance in ectotherms. In: Wang LCH (ed) Advances in Comparative and Environmental Physiology, vol 4. Springer, Berlin, pp 51–82Google Scholar
  121. Storey KB, Storey JM (1990) Facultative metabolic rate depression: molecular regulation and biochemical adaptation in anaerobiosis, hibernation and aestivation. Q Rev Biol 65:145–174PubMedGoogle Scholar
  122. Storey KB, Storey JM (1991) Biochemistry of cryoprotectants. In: Denlinger DL, Lees RE (eds) Insects at Low Temperatures. Chapman, New York, pp 64–93Google Scholar
  123. Storey KB, Storey JM (1996) Natural freezing survival in animals. Annu Rev Ecol Syst 27:365–386Google Scholar
  124. Storey KB, Storey JM, Brooks SP, Churchill TA, Brooks RJ (1988) Hatchling turtles survive freezing during winter hibernation. Proc Natl Acad Sci USA 85:8350–8354PubMedGoogle Scholar
  125. Taplin LE (1988) Osmoregulation in crocodilians. Biol Rev 63:333–377Google Scholar
  126. Thomas DW, Geiser F (1997) Periodic arousals in hibernating mammals: is evaporative water loss involved? Funct Ecol 11:585–591Google Scholar
  127. Tunnacliffe A, Lapinski J (2003) Resurrecting van Leeuwenhoek’s rotifers: a reappraisal of the role of disaccharides in anhydrobiosis. Philos Trans R Soc London B 358:1755–1771Google Scholar
  128. Turner JH (1933) The viability of seeds. Kew Bull 6:251Google Scholar
  129. Van Beurden E (1980) Energy metabolism of dormant Australian water-holding frogs (Cyclorana platycephala). Copeia 1980:787–799Google Scholar
  130. Van Gundy SD (1965) Factors in survival of nematodes. Annu Rev Phytopathol 3:43–68Google Scholar
  131. Van Leeuwenhoek A (1702) On certain animalcules found in the sediments in gutter of the roofs of houses. Letter 144, to Hendrik van Bleyswijk. In: Selected Works of Anton van Leeuwenhoek, vol 2. London. pp. 207–213Google Scholar
  132. Watanabe M (2006) Anhydrobiosis in invertebrates. Appl Entomol Zool 41:15–31Google Scholar
  133. Weigmann R (1929) Die Wirkung starker Abkfihlung auf Amphibien und Reptitien. Z Wiss Zool 134:641–692Google Scholar
  134. Wharton DA (2002) Life at the limits. Organisms in extreme environments. Cambridge University Press, CambridgeGoogle Scholar
  135. Withers PC (1992) Comparative animal physiology. Saunders College Publishing, PhiladelphiaGoogle Scholar
  136. Withers PC (1993) Metabolic depression during aestivation in the Australian frogs, Neobatrachus and Cyclorana. Aust J Zool 41:467–473Google Scholar
  137. Womersley C (1981) Biochemical and physiological aspects of anhydrobiosis. Comp Biochem Physiol B 70:668–678Google Scholar
  138. Wright JC (2001) Cryptobiosis 300 years on from van Leuwenhoek: what have we learned about tardigrades? Zool Anz 240:563–582Google Scholar
  139. Wright JC, Westh P, Ramløv H (1992) Cryptobiosis in Tardigrada. Biol Rev 67:1–29Google Scholar
  140. Zachariassen KE (1985) Physiology of cold tolerance in insects. Physiol Rev 65:799–832PubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Zoology, School of Animal Biology M092University of Western AustraliaCrawleyAustralia
  2. 2.Department of Environmental and Aquatic ScienceCurtin University of TechnologyPerthAustralia

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